Repeated restraint stress enhances cue-elicited conditioned freezing and impairs acquisition of extinction in an age-dependent manner

Behavioural Brain Research

Volumn 248, Issue , 2013, Pages 12-24

  Zhang, Wei ^a   Rosenkranz, J Amiel ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Adolescent; Amygdala; Chronic stress; Fear conditioning; Fear extinction; Repeated restraint

Indexed keywords

ADOLESCENT; ADULT ANIMAL; AGE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY FEAR CONDITIONING; CHRONIC STRESS; CONDITIONING; CONTROLLED STUDY; FEAR; IMMOBILIZATION STRESS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

AGING; AMYGDALA; ANIMALS; ANXIETY; CONDITIONING (PSYCHOLOGY); CUES; EXTINCTION, PSYCHOLOGICAL; FEAR; FREEZING; MALE; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL;

EID: 84877013915     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.03.028     Document Type: Article

References (89)

1. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biological Psychiatry 2001, 49:1023-1039.
2. Yehuda R. Post-traumatic stress disorder. New England Journal of Medicine 2002, 346:108-114.
3. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience 2009, 10:434-445.
4. Davis M., Rainnie D., Cassell M. Neurotransmission in the rat amygdala related to fear and anxiety. Trends in Neurosciences 1994, 17:208-214.
5. Davis M. The role of the amygdala in conditioned and unconditioned fear and anxiety. The amygdala: a functional analysis 2000, 213-287. Oxford UP. J.P. Aggleton (Ed.).
6. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends in Neurosciences 1997, 20:78-84.
7. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 2000, 23:155-184.
8. Kaufman J., Plotsky P.M., Nemeroff C.B., Charney D.S. Effects of early adverse experiences on brain structure and function: clinical implications. Biological Psychiatry 2000, 48:778-790.
9. Teicher M.H., Andersen S.L., Polcari A., Anderson C.M., Navalta C.P., Kim D.M. The neurobiological consequences of early stress and childhood maltreatment. Neuroscience and Biobehavioral Reviews 2003, 27:33-44.
10. Vyas A., Mitra R., Shankaranarayana Rao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience 2002, 22:6810-6818.
11. Mitra R., Jadhav S., McEwen B.S., Vyas A., Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:9371-9376.
12. Correll C.M., Rosenkranz J.A., Grace A.A. Chronic cold stress alters prefrontal cortical modulation of amygdala neuronal activity in rats. Biological Psychiatry 2005, 58:382-391.
13. Rosenkranz J.A., Venheim E.R., Padival M. Chronic stress causes amygdala hyperexcitability in rodents. Biological Psychiatry 2010, 67:1128-1136.
14. Vyas A., Pillai A.G., Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
15. Chiba S., Numakawa T., Ninomiya M., Richards M.C., Wakabayashi C., Kunugi H. Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2012, 39:112-119.
16. Conrad C.D., LeDoux J.E., Magariños A.M., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behavioral Neuroscience 1999, 113:902-913.
17. Atchley D., Hankosky E.R., Gasparotto K., Rosenkranz J.A. Pharmacological enhancement of calcium-activated potassium channel function reduces the effects of repeated stress on fear memory. Behavioural Brain Research 2012, 232:37-43.
18. Drevets W.C. Prefrontal cortical-amygdalar metabolism in major depression. Annals of the New York Academy of Sciences 1999, 877:614-637.
19. Drevets W.C., Price J.L., Furey M.L. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Structure & Function 2008, 213:93-118.
20. Villarreal G., King C.Y. Brain imaging in posttraumatic stress disorder. Seminars in Clinical Neuropsychiatry 2001, 6:131-145.
21. Davidson R.J. Affective neuroscience and psychophysiology: toward a synthesis. Psychophysiology 2003, 40:655-665.
22. Spear L.P., Brake S.C. Periadolescence: age-dependent behavior and psychopharmacological responsivity in rats. Developmental Psychobiology 1983, 16:83-109.
23. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews 2000, 24:417-463.
24. Sisk C.L., Foster D.L. The neural basis of puberty and adolescence. Nature Neuroscience 2004, 7:1040-1047.
25. Gabriel S.M., Roncancio J.R., Ruiz N.S. Growth hormone pulsatility and the endocrine milieu during sexual maturation in male and female rats. Neuroendocrinology 1992, 56:619-625.
26. Zanato V.F., Martins M.P., Anselmo-Franci J.A., Petenusci S.O., Lamano-Carvalho T.L. Sexual development of male Wistar rats. Brazilian Journal of Medical and Biological Research 1994, 27:1273-1280.
27. Zhang W., Rosenkranz A.J. Repeated restraint stress increases basolateral amygdala neuronal activity in an age-dependent manner. Neuroscience 2012, 226:459-474.
28. Goosens K.A., Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learning and Memory 2001, 8:148-155.
29. Maren S. Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience 2001, 24:897-931.
30. Toledo-Rodriguez M., Sandi C. Stress before puberty exerts a sex- and age-related impact on auditory and contextual fear conditioning in the rat. Neural Plasticity 2007, 71203.
31. Kant G.J., Eggleston T., Landman-Roberts L., Kenion C.C., Driver G.C., Meyerhoff J.L. Habituation to repeated stress is stressor specific. Pharmacology Biochemistry and Behavior 1985, 22:631-634.
32. Stamp J.A., Herbert J. Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress. Neuroscience 1999, 94:1313-1322.
33. Doremus-Fitzwater T.L., Varlinskaya E.I., Spear L.P. Factor analysis of elevated plus-maze behavior in adolescent and adult rats. Pharmacology Biochemistry and Behavior 2006, 83:570-577.
34. Doremus-Fitzwater T.L., Varlinskaya E.I., Social Spear L.P. non-social anxiety in adolescent and adult rats after repeated restraint. Physiology and Behavior 2009, 97:484-494.
35. Lynn D.A., Brown G.R. The ontogeny of anxiety-like behavior in rats from adolescence to adulthood. Developmental Psychobiology 2010, 52:731-739.
36. Davis M. Neurobiology of fear responses: the role of the amygdala. Journal of Neuropsychiatry and Clinical Neurosciences 1997, 9:382-402.
37. Maren S., Aharonov G., Stote D.L., Fanselow M.S. N-methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats. Behavioral Neuroscience 1996, 110:1365-1374.
38. Muller J., Corodimas K.P., Fridel Z., LeDoux J.E. Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behavioral Neuroscience 1997, 111:683-691.
39. Fendt M., Fanselow M.S. The neuroanatomical and neurochemical basis of conditioned fear. Neuroscience and Biobehavioral Reviews 1999, 23:743-760.
40. Wilensky A.E., Schafe G.E., LeDoux J.E. Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. Journal of Neuroscience 1999, 19:RC48.
41. Roozendaal B., Barsegyan A., Lee S. Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Progress in Brain Research 2008, 167:79-97.
42. Labar K.S., LeDoux J.E., Spencer D.D., Phelps E.A. Impaired fear conditioning following unilateral temporal lobectomy in humans. Journal of Neuroscience 1995, 15:6846-6855.
43. Knight D.C., Smith C.N., Stein E.A., Helmstetter F.J. Functional MRI of human Pavlovian fear conditioning: patterns of activation as a function of learning. Neuroreport 1999, 10:3665-3670.
44. LaBar K.S., Gatenby J.C., Gore J.C., LeDoux J.E., Phelps E.A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 1998, 20:937-945.
45. Groves P.M., Thompson R.F. Habituation: a dual-process theory. Psychological Review 1970, 77:419-450.
46. Davis M. Sensitization of the acoustic startle reflex by footshock. Behavioral Neuroscience 1989, 103:495-503.
47. Kendig M.D., Bowen M.T., Kemp A.H., McGregor I.S. Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience. Behavioural Brain Research 2011, 225:405-414.
48. Morrissey M.D., Mathews I.Z., McCormick C.M. Enduring deficits in contextual and auditory fear conditioning after adolescent, not adult, social instability stress in male rats. Neurobiology of Learning and Memory 2011, 95:46-56.
49. Yee N., Schwarting R.K., Fuchs E., Wöhr M. Juvenile stress potentiates aversive 22-kHz ultrasonic vocalizations and freezing during auditory fear conditioning in adult male rats. Stress 2012, 15:533-544.
50. Garcia R., Spennato G., Nilsson-Todd L., Moreau J.L., Deschaux O. Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats. Neurobiology of Learning and Memory 2008, 89:560-566.
51. Vyas A., Jadhav S., Chattarji S. Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 2006, 143:387-393.
52. Chalmers D.T., Lovenberg T.W., De Souza E.B. Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1, receptor mRNA Expression. Journal of Neuroscience 1995, 15:6340-6350.
53. Chen Y., Brunson K.L., Muller M.B., Cariaga W., Baram T.Z. Immuno- cytochemical distribution of corticotropin-releasing hormone receptor type-1 (CRF(1))-like immunoreactivity in the mouse brain: light microscopy analysis using an antibody directed against the C-terminus. Journal of Comparative Neurology 2000, 420:305-323.
54. Rainnie D.G., Fernhout B.J., Shinnick-Gallagher P. Differential actions of corticotropin releasing factor on basolateral and central amygdaloid neurones, in vitro. Journal of Pharmacology and Experimental Therapeutics 1992, 263:846-858.
55. Rainnie D.G., Bergeron R., Sajdyk T.J., Patil M., Gehlert D.R., Shekhar A. Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. Journal of Neuroscience 2004, 24:3471-3479.
56. Nemeroff C.B., Widerlöv E., Bissette G., Walléus H., Karlsson I., Eklund K., et al. Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science 1984, 226:1342-1344.
57. Koob G.F., Heinrichs S.C. A role for corticotropin releasing factor and urocortin in behavioral responses to stressors. Brain Research 1999, 848:141-152.
58. Yehuda R., Teicher M.H., Trestman R.L., Levengood R.A., Siever L.J. Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biological Psychiatry 1996, 40:79-88.
59. Jedema H.P., Sved A.F., Zigmond M.J., Finlay J.M. Sensitization of norepinephrine release in medial prefrontal cortex: effect of different chronic stress protocols. Brain Research 1999, 830:211-217.
60. Bland S.T., Twining C., Watkins L.R., Maier S.F. Stressor controllability modulates stress-induced serotonin but not dopamine efflux in the nucleus accumbens shell. Synapse 2003, 49:206-208.
61. Buffalari D.M., Grace A.A. Chronic cold stress increases excitatory effects of norepinephrine on spontaneous and evoked activity of basolateral amygdala neurons. International Journal of Neuropsychopharmacology 2009, 12:95-107.
62. Rasheed N., Ahmad A., Pandey C.P., Chaturvedi R.K., Lohani M., Palit G. Differential response of central dopaminergic system in acute and chronic unpredictable stress models in rats. Neurochemical Research 2010, 35:22-32.
63. Yohe L.R., Suzuki H., Lucas L.R. Aggression is suppressed by acute stress but induced by chronic stress: immobilization effects on aggression, hormones, and cortical 5-HT(1B)/striatal dopamine D(2) receptor density. Cognitive, Affective, & Behavioral Neuroscience 2012, 12:446-459.
64. Miracle A.D., Brace M.F., Huyck K.D., Singler S.A., Wellman C.L. Chronic stress impairs recall of extinction of conditioned fear. Neurobiology of Learning and Memory 2006, 85:213-218.
65. Quirk G.J., Garcia R., González-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry 2006, 60:337-343.
66. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
67. Giedd J.N., Vaituzis A.C., Hamburger S.D., Lange N., Rajapakse J.C., Kaysen D., et al. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. Journal of Comparative Neurology 1996, 366:223-230.
68. Sowell E.R., Thompson P.M., Tessner K.D., Toga A.W. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. Journal of Neuroscience 2001, 21:8819-8829.
69. Markham J.A., Morris J.R., Juraska J.M. Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 2007, 144:961-968.
70. Chareyron L.J., Lavenex P.B., Lavenex P. Postnatal development of the amygdala: a stereological study in rats. Journal of Comparative Neurology 2012, 520:3745-3763.
71. Poeggel G., Helmeke C., Abraham A., Schwabe T., Friedrich P., Braun K. Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:16137-16142.
72. Silva-Gómez A.B., Rojas D., Juárez I., Flores G. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Research 2003, 983:128-136.
73. Teicher H.M. Childhood abuse and regional brain development: evidence for sensitive periods. American Academy of Child & Adolescent Psychiatry 2005, 25:78. (Toronto, Ontario).
74. Jacobson-Pick S., Elkobi A., Vander S., Rosenblum K., Richter-Levin G. Juvenile stress-induced alteration of maturation of the GABAA receptor alpha subunit in the rat. International Journal of Neuropsychopharmacology 2008, 11:891-903.
75. Cressman V.L., Balaban J., Steinfeld S., Shemyakin A., Graham P., Parisot N., et al. Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat. Journal of Comparative Neurology 2010, 518:2693-2709.
76. Hefner K., Holmes A. Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behavioural Brain Research 2007, 176:210-215.
77. Pattwell S.S., Duhoux S., Hartley C.A., Johnson D.C., Jing D., Elliott M.D., et al. Altered fear learning across development in both mouse and human. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:16318-16323.
78. McKinzie D.L., Chen W.J., Spear N.E. Ontogenetic differences in the expression of conditioned stimulus conditioning: effects of retention interval. Behavioral Neuroscience 1998, 112:920-928.
79. Stanton M.E., Freeman J.H., Skelton R.W. Eyeblink conditioning in the developing rat. Behavioral Neuroscience 1992, 106:657-665.
80. Rudy J.W. Contextual conditioning and auditory cue conditioning dissociate during development. Behavioral Neuroscience 1993, 107:887-891.
81. Mckinzie D.L., Spear N.E. Ontogenetic differences in conditioning to context and CS as a function of context saliency and CS-US interval. Learning & Behavior 1995, 23:304-313.
82. Esmorís-arranz F.J., Spear N.E. Contextual fear conditioning differs for infant, adolescent, and adult rats. Behav Presses 2008, 78:340-350.
83. Barnet R.C., Hunt P.S. The expression of fear-potentiated startle during development: integration of learning and response systems. Behavioral Neuroscience 2006, 120:861-872.
84. Yap C.S., Richardson R. The ontogeny of fear-potentiated startle: effects of earlier-acquired fear memories. Behavioral Neuroscience 2007, 121:1053-1062.
85. Li S., Kim J.H., Richardson R. Differential involvement of the medial prefrontal cortex in the expression of learned fear across development. Behavioral Neuroscience 2012, 126:217-225.
86. Kim J.H., Hamlin A.S., Richardson R. Fear extinction across development: the involvement of the medial prefrontal cortex as assessed by temporary inactivation and immunohistochemistry. Journal of Neuroscience 2009, 29:10802-10808.
87. Pan B.X., Ito W., Morozov A. Divergence between thalamic and cortical inputs to lateral amygdala during juvenile-adult transition in mice. Biological Psychiatry 2009, 66:964-971.
88. Brummelte S., Witte V., Teuchert-Noodt G. Postnatal development of GABA and calbindin cells and fibers in the prefrontal cortex and basolateral amygdala of gerbils (Meriones unguiculatus). International Journal of Developmental Neuroscience 2007, 25:191-200.
89. Dávila J.C., Olmos L., Legaz I., Medina L., Guirado S., Real M.A. Dynamic patterns of colocalization of calbindin, parvalbumin and GABA in subpopulations of mouse basolateral amygdalar cells during development. Journal of Chemical Neuroanatomy 2008, 35:67-76.